ORIGINAL RESEARCH ARTICLE
published: 15 January 2009
Stress effects on working memory, explicit memory, and
implicit memory for neutral and emotional stimuli in
Mathias Luethi1, Beat Meier1* and Carmen Sandi2
Department of Psychology, University of Bern, Bern, Switzerland
Laboratory of Behavioral Genetics, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Switzerland
Stress is a strong modulator of memory function. However, memory is not a unitary process 7
Sonia Lupien, McGill University,
and stress seems to exert different effects depending on the memory type under study. Here, 8
we explored the impact of social stress on different aspects of human memory, including tests 9
for explicit memory and working memory (for neutral materials), as well as implicit memory
Tony W. Buchanan, Saint Louis
(perceptual priming, contextual priming and classical conditioning for emotional stimuli). A total 11
Dominique J. F. de Quervain, University
of 35 young adult male students were randomly assigned to either the stress or the control 12
of Zurich, Switzerland
group, with stress being induced by the Trier Social Stress Test (TSST). Salivary cortisol levels 13
were assessed repeatedly throughout the experiment to validate stress effects. The results 14
Beat Meier, Department of Psychology,
support previous evidence indicating complex effects of stress on different types of memory:
University of Bern, Muesmattstr. 45,
CH-3000 Bern 9, Switzerland.
A pronounced working memory de? cit was associated with exposure to stress. No performance 16
differences between groups of stressed and unstressed subjects were observed in verbal explicit 17
memory (but note that learning and recall took place within 1 h and immediately following stress) 18
or in implicit memory for neutral stimuli. Stress enhanced classical conditioning for negative 19
but not positive stimuli. In addition, stress improved spatial explicit memory. These results 20
reinforce the view that acute stress can be highly disruptive for working memory processing. 21
They provide new evidence for the facilitating effects of stress on implicit memory for negative 22
emotional materials. Our ? ndings are discussed with respect to their potential relevance for 23
psychiatric disorders, such as post traumatic stress disorder.
Keywords: stress, cortisol, implicit memory, working memory, conditioning, emotional stimuli
administration and as a result of psychological stress (Kirschbaum 50
There is substantial evidence that stress and enhanced glucocorti-
et al., 1996; Lupien et al., 1999; Newcomer et al., 1994, 1999; Oei 51
coid levels can have complex in? uences on memory performance,
et al., 2006; Payne et al., 2007). However, there are also examples in 52
with both negative and positive consequences (Lupien and Lepage,
which a potentation of memory was observed after corticosterone 53
2001; Lupien et al., 2007; Sandi and Pinelo-Nava, 2007; Wolf, 2003).
treatment (Buchanan and Lovallo, 2001; Putman et al., 2004) or 54
Critical brain areas for cognition and emotion – such as the hip-
when psychological stress was applied before (Payne et al., 2007) 55
pocampus and the amygdala in rodents, and the hippocampus and
or after (Smeets et al., 2008) training. For implicit memory, the 56
frontal lobe in humans – contain a high density of glucocorticoid
small number of studies that have addressed this issue suggest that 57
receptors (de Kloet et al., 1999; Lupien and McEwen, 1997).
performance is unaffected by stress and elevated cortisol levels 58
In rodents, converging evidence suggests that stress effects on (Kirschbaum et al., 1996; Lupien et al., 1997).
hippocampus- and prefrontal cortex-dependent memory follow an
One of the key issues addressed in recent years has been the 60
inverted U-shaped function, with moderate stress levels facilitating,
potentially different susceptibility of different memory phases 61
while high levels impairing, memory function (Cordero and Sandi,
(i.e., acquisition, consolidation, retrieval) to the effects of acute 62
1998; Del Arco et al., 2007; Sandi and Pinelo-Nava, 2007; Sandi stress and increased cortisol levels (Roozendaal et al., 2002; Smeets 63
et al., 1997; Selden et al., 1990). Glucocorticoids seem to play a key
et al., 2008). Evidence from studies on explicit memory suggest 64
role in these stress effects, since an inverted U-shaped function has
that retrieval processes are particularly susceptible to the adverse 65
also been reported for the relationship between glucocorticoid lev-
effects of acute stress and increased cortisol, while consolidation 66
els and memory and plasticity (Abrari et al., 2008; Joëls, 2006; Sandi
processes could be in fact potentiated by both stress and glucocorti- 67
and Rose, 1997). Conversely, hippocampus-independent memory
coids (Beckner et al., 2006; de Quervain et al., 2000; Het et al., 2005; 68
is frequently facilitated by stress (Sandi and Pinelo-Nava, 2007; Lupien and Schramek, 2006; Roozendaal et al., 2002).
Shors, 2004, 2006), and this facilitation seems to be dependent on
Another key issue has been to ascertain whether the emotional 70
glucocorticoids (Shors, 2001; Shors and Beylin, 2003).
modulation of memory formation – in which amygdala activa- 71
In humans, explicit memory and working memory formation tion has been critically involved (Cahill, 2003) – occurs for both 72
have been shown to be frequently impaired after corticosteroid positive and negative materials. Findings in rodents suggest that 73
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Stress effects on memory
the enhancing effect of glucocorticoids on memory consolidation
SALIVA SAMPLING AND FREE CORTISOL ANALYSIS
depend on emotional arousal (e.g., Roozendaal et al., 2006). In Saliva was collected using Salivette (Sarstedt, Sevelen, Switzerland) 131
humans, a memory bias towards negative stimuli is often described
collection devices. Saliva samples were taken at the end of a relaxa- 132
in patients whose condition is associated with elevated levels of tion phase to assess baseline cortisol levels (sample 1); and 15 min 133
stress hormones (Colombel, 2007; Elzinga and Bremner, 2002; after stress cessation, or 15 min after the beginning of memory 134
Moradi et al., 2000; Rinck and Becker, 2005; Watkins et al., 2000).
testing in controls to assess peak levels or comparison levels, respec- 135
In a recent study (Abercrombie et al., 2006), high cortisol output tively (sample 2). Sample 3 was taken at the end of the memory 136
during a social stressor was related to memory facilitation in sub-
testing phase. Samples were stored at ?30°C until analysis. Cortisol 137
jects who reported high stress-related negative affect, and this rela-
concentration was measured using the Spectria Cortisol radio- 138
tion was especially prominent for recall of unpleasant information.
immunoassay RIA commercial kit (Orion Diagnostica, Espoo, 139
Other studies also found impaired recall for negative and positive
words, but no effect for neutral words (Kuhlmann et al., 2005; Tops
et al., 2003). In accordance with ? ndings in rodents, stress induced
facilitation of the implicit learning of emotionally negative infor-
Subjects were tested individually in the second half of the day 142
mation was also found in humans (Gidron et al., 2002). Similarly,
between 11 a.m.–1 p.m. (n = 9), 2–4 p.m. (n = 14) or 4–6 p.m. 143
Jackson et al. (2006) report enhanced fear conditioning after stress
(n = 12). Test sessions lasted 1½–2 h and consisted of a relaxation 144
exposure in men, but not in women. This effect was associated with
phase (25 min), exposure to a social stressor (25 min; only for the 145
elevated cortisol levels. Interestingly, the impairing effects of gluco-
stress group) and a memory testing phase (1 h). After comple- 146
corticoids on memory retrieval seem to also depend on emotional
tion of a post-experimental questionnaire, subjects were debriefed. 147
arousal (e.g., Roozendaal et al., 2006) both for positive and negative
Controls started memory testing immediately after the relaxation 148
information (de Quervain et al., 2007).
phase. Table 1 shows an overview of the order of the speci? c tasks 149
The aim of this study was to assess the effects of stress and cor-
tisol on a comprehensive variety of memory tasks in male human
subjects, including tests for explicit memory (for neutral materials),
working memory, and implicit memory (perceptual and contextual
After arrival at the laboratory (t0), subjects rested while completing 152
priming and classical conditioning for emotional stimuli), with a socio demographic-questionnaire. They were instructed to take as 153
100 a particular focus on different types of implicit memory. Stress much time as they needed to answer the questions. In case subjects 154
101 was induced in half of the sample through the Trier social stress did not manage to complete the questionnaire within 30 min, they 155
102 test (TSST; Kirschbaum et al., 1993). Explicit memory was stud-
were told to stop (t30), see Table 1.
103 ied through a standardized explicit memory test (LGT-3; Bäumler,
104 1974). Working memory was assessed with the reading span task Stress exposure
105 (Daneman and Carpenter, 1980). For implicit memory, a perceptual Subjects in the stress group were exposed to the Trier Social Stress Test 158
106 priming task, a contextual priming task, and a conditioning task (TSST; Kirschbaum et al., 1993) at t30 (see Table 1). Subjects were 159
107 were used. The priming tasks consisted of neutral materials, while told that the TSST procedure is about simulating a job interview. The 160
108 the conditioning task included both positive and negative stimuli. TSST mainly consists of a stress anticipation period, a free speech 161
109 To validate the effects of social stress, salivary cortisol was sampled and mental arithmetic task to be performed in front of an audience. 162
110 repeatedly throughout the experiment. Based on previous ? ndings, Members of the “audience” (these were colleagues of the ? rst author) 163
111 we expected a negative effect of stress on explicit memory and were introduced as being trained in observing nonverbal behaviour. 164
112 working memory. In contrast, we did not expect stress effects on Subjects had to stand close to a microphone and a video camera. They 165
113 implicit memory for non-emotional materials, but hypothesized were told that their performance would be videotaped for subsequent 166
114 facilitative effect of stress on implicit memory for the condition analysis. A powerful light source was directed towards the subjects 167
115 with emotionally congruent materials.
and they saw themselves on a monitor screen connected to the video 168
camera. During performance subjects were given negative feedback 169
116 MATERIALS AND METHODS
about their level of achievement by the audience.
117 SUBJECTS AND DESIGN
118 Thirty-? ve healthy male volunteers, aged 23.4 ± 2.9 years (M ± SD), MEMORY TESTS
119 range 20–34 years, participated in this study. They were randomly Explicit memory
120 assigned to either the stress (n = 19) or the control group (n = 16). Explicit memory was assessed using two sub-tests of a standardized 173
121 Groups did not differ with respect to age or education level.
memory test (LGT-3; Bäumler, 1974). The ? rst test was a verbal 174
All subjects were informed that the experiment might be partly
memory test. Subjects were presented with a list of 20 German 175
123 unpleasant and that they were free to leave at any time. They signed and Turkish words (stress group: t60/control group: t30). They 176
124 a consent form prior to testing. All subjects were medication-free. At were instructed to learn both the German words and the Turkish 177
125 least 1 h prior to testing (1½ h prior to the ? rst saliva sample), par-
translations and were given 1 min to study the list. The second test 178
126 ticipants refrained from exercise, smoking (smoking > 10 cigarettes/
was a spatial memory test. Subjects were instructed to learn a route 179
127 day was an exclusion criteria), eating, or drinking alcoholic beverages on a map (t61/t31). They were also given 1 min for study. Free recall 180
128 or low pH soft drinks. Each subject completed a questionnaire to and recognition were tested at t113–116 in the stress group, and 181
129 con? rm good health and compliance with dietary instructions.
t83–86 in the control group, respectively (see Table 1).
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Table 1 | Ordering of tasks and activities.
Explicit memory study
t 60–61 t
t 61–62 t
Classical conditioning study
t 62–74 t
Perceptual priming study
t 74–78 t
Contextual priming task
t 78–90 t
Classical conditioning evaluation
t 90–92 t
Perceptual priming test
t 92–99 t
t 99–113 t
t 113–115 t
t 115–116 t
END OF MEMORY TESTING
t 116 t
t > 116
t > 86
t > 116
t > 86
183 Working memory
(study phase; t74–78/t44–48). Each display was presented for 1 s, 211
184 Working memory was assessed with a modi? ed version of the reading followed by a blank screen, during which subjects responded. After 212
185 span task (Daneman and Carpenter, 1980). Subjects were instructed a ? lled delay, subjects were given a fragmented pictures test (t92–99/ 213
186 to read aloud a set of sentences and to indicate whether they were t62–69; see Table 1). A total of 100 pictures were presented in ran- 214
187 meaningful. In addition, they were also instructed to memorize the dom order. Half of them were previously shown and half were new 215
188 last word of each sentence and to recall these last words in the correct objects. Subjects were instructed to name each object. They were 216
189 order at the end of a trial. Trials consisted of sets of two, three, four, also informed that objects would be dif? cult to identify because 217
190 ? ve or six sentences. There were ? ve trials for each set size. After they were shown in fragmented form. First, the most fragmented 218
191 a practice trial, the test trials started with sets of two sentences. If version of an object was shown for 3 s. If the subject was unable to 219
192 the subject was able to recall all the words in at least one of the ? ve name the object correctly, the same object was presented in a less 220
193 trials, ? ve trials with three sentences were presented, etc. If subjects fragmented version. This procedure was repeated until the object 221
194 failed to recall all the words of a given set size in at least one trial of was named correctly. If an object was identi? ed correctly, the next 222
195 a given set size, the task was stopped. Reading span was de? ned as object appeared on the screen, again in its most fragmented version 223
196 the size of the largest set in which all words were correctly recalled ? rst. The level of picture fragmentation, at which an object was 224
197 in at least three of the ? ve trials. If subjects correctly recalled all identi? ed, was recorded. For each object, six fragmentation levels 225
198 words of two sets at a given set size, the reading span was scored as were used with objects being complete in the last version. The four 226
199 the size of this set minus 0.5 (cf. Daneman and Carpenter, 1980). lists of items were counterbalanced across conditions. Priming was 227
200 Working memory was assessed at t99–113 in the stress group and calculated as the difference between the fragmentation level at which 228
201 t69–83 in the control group (see Table 1).
old (i.e., previously seen) and new drawings were identi? ed.
202 Perceptual priming
203 Perceptual priming was assessed with a fragmented pictures test Contextual priming was assessed with a paradigm from Chun and 231
204 (cf. Meier, 2001; Meier et al., 2009). A total of 100 line drawings Jiang (1998; t78–90/t48–60, see Table 1). Materials consisted of a total 232
205 of common objects from materials of Snodgrass and Vanderwart of 90 search displays presented on a computer screen. Each display 233
206 (1980) were used. They were presented in black against a white featured 12 coloured items presented in a small square (4 × 2.5 cm) 234
207 background on a computer screen. Four groups of 25 line-drawings against a grey background. There were equal numbers of red, green, 235
208 were composed such that each group had the same baseline comple-
blue and yellow items in each display. Each display consisted of 11 236
209 tion rate. During study two sets of 25 line drawings were presented distracters and 1 target item that appeared anywhere within a grid of 237
210 and participants were instructed to perform a simple decision task 8 × 6 locations. Distracter items were L – letters, which were rotated 238
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239 through 0, 90, 180 or 270 degrees. The target item was a T, which was neg characters. CS-US covariation awareness was controlled using 295
240 rotated through 90 degrees either in clockwise or counter-clockwise a funnelled multiple-choice questionnaire at the end of the testing 296
241 direction. In each block, ? ve “new” displays and ? ve “old” displays phase (t116/t86, see Table 1).
242 were shown in randomised order. Each type of “old” display was
243 presented once in a block, and eight times across the experiment. STATISTICS
244 Within each “old” display, the spatial and colour con? guration of the Results are expressed as mean (M) ± standard deviation (SD). 299
245 items was the same. Hence, over the repetitions, the visual context Mean differences between the two groups were assessed by means 300
246 predicted the location of the target item as “old” displays differed of Student t-tests. Signi? cance was considered at p < 0.05.
247 only with respect to the orientation of the target item. “New” displays
248 differed with respect to both the spatial and colour con? gurations of RESULTS
249 the items. Each trial began with the presentation of a ? xation cross SALIVARY CORTISOL LEVELS
250 and after a 500-ms delay, a visual search display appeared. Subjects Salivary cortisol levels did not differ between the stress and control 304
251 were instructed to indicate as quickly and accurately as possible group at baseline (M = 10.0 nmol/L, SD = 3.9 vs. M = 8.6 nmol/L, 305
252 the direction of the T-base. The visual search display disappeared SD = 4.7), but they were elevated in the stress group 15 min after 306
253 if one of the response keys was pressed, or after a maximum of 6 s. the beginning of the testing phase [M = 23.2 nmol/L, SD = 13.6 vs. 307
254 The next trial was initiated 1000 ms after response. Feedback was M = 9.6 nmol/L, SD = 3.2; t(20.5) = 4.2, p < 0.001] and at the end of 308
255 given for incorrect responses. Priming was assessed as differential the testing phase [M = 15.6 nmol/L, SD = 7.2 vs. M = 10.6 nmol/L, 309
256 speed-up in RTs for old vs. new items across blocks. For analysis SD = 3.2; t(26) = 2.7, p = 0.01]. Salivary cortisol levels rose signi? - 310
257 Blocks 1 and 2, Blocks 3 and 4, Blocks 5 and 6, and Blocks 7 and cantly in response to the TSST [t(18) = ?4.1, p = 0.001], whereas 311
258 8 were summarized as Epoch 1 to 4 in order to enhance statistical controls showed no difference in cortisol levels between sam- 312
259 power. At t116/t86, subjects were asked whether they were aware of ples 1 and 2. The mean cortisol increase (sample 2–sample 1) in 313
260 repeated presentation of “old” displays (see Table 1). Additionally, the experimental group was 13.1 nmol/L. The increase in cortisol 314
261 a recognition test featuring “old” and “new” displays as well as dis-
concentration could not be calculated in one control subjects due 315
262 plays not used in the experiment was conducted to test for explicit to an insuf? cient amount of saliva.
263 learning of stimulus con? gurations.
Cortisol has a pronounced diurnal pattern. Accordingly, the base- 317
line cortisol concentration tended to differ between the different 318
264 Classical conditioning
testing times in the afternoon [F(2, 32) = 2.7, p = 0.08]. However, the 319
265 To assess conditioning for emotional material a paradigm by Olson baseline cortisol concentration was not associated with the increase 320
266 and Fazio (2001) was used. Subjects were told that the task was about in cortisol concentration, nor did the cortisol response differ between 321
267 “video surveillance”, and that several hundred pictures would be subjects with low vs. high cortisol concentrations at baseline (groups 322
268 presented on a computer screen (t62–74/t32–44, see Table 1). They based on median cortisol level = 7.58 nmol/L). These results validate 323
269 were instructed to hit a response key as quickly as possible when a the ef? cacy of the TSST in inducing stress. There was a clear-cut 324
270 target appeared. Target events were de? ned as a name or a picture endocrine response to the psychological stressor which was not sig- 325
271 of a Pokemon cartoon character. They could appear either alone ni? cantly in? uenced by the cortisol concentration at baseline.
272 or paired with other photographs or other words. Subjects were
273 told to focus on monitoring for targets and not to get distracted MEMORY TESTS
274 by the other items. These ? ller items consisted of other Pokemon Descriptive statistics for all memory tests are presented in Table 2. 328
275 ? gures or names, blank screens, and neutrally valenced words and For all statistical analyses an alpha-level of 0.05 was used. Due to an 329
276 pictures (see Olson and Fazio, 2001). A total of ? ve blocks, each experimenter error, working memory data of one control and two 330
277 consisting of 86 trials, was administered. Eight pairs of conditioned stressed subjects and verbal explicit memory data of one control 331
278 stimuli (CS) and unconditioned stimuli (UCS) were presented in subject had to be excluded from analysis.
279 each block. These pairs consisted of a Pokemon character and a
280 positively valenced word (e.g., “excellent”) or picture (e.g., a puppy) Explicit memory
281 and another Pokemon cartoon character paired with a negative Measures of the verbal explicit memory test were indistinguish- 334
282 word (e.g., “terrible”) or picture (e.g., a cockroach). Following the able between the stress and the control group. Subjects in the 335
283 procedure of Olson and Fazio, the pokemon characters Shelder stress group achieved higher scores in the spatial memory test 336
284 and Metapod were used as CSs. Pokemon character and US were [t(33) = 2.1, p = 0.046].
285 counterbalanced across conditions. After the conditioning phase,
286 subjects were asked to complete a picture evaluation task (t90 or Working memory
287 t60, respectively). They were told that one purpose of this task Subjects exposed to the TSST had a lower reading span 339
288 was to control for interference effects of some ? ller items. Thirty [t(28.5) = ?2.1, p = 0.046] as well as signi? cantly lower total cor- 340
289 photographs and Pokemon characters, including the “positive” rect scores [t(30) = ?2.4, p = 0.023] relative to controls. The results 341
290 CS (CS pos) and the “negative” CS (CS neg) were presented at a suggest a stress-induced working memory impairment.
291 rapid pace on the computer screen. Subjects were asked to evalu-
292 ate the pictures on a scale ranging from extremely negative (?4) Perceptual priming
293 to extremely positive (+4) as quickly as possible. A conditioning Lower mean fragmentation levels at which objects were cor- 344
294 effect was de? ned as a more positive rating of CS pos relative to CS rectly identi? ed, indicate higher levels of object fragmentation 345
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Table 2 | Descriptive statistics indicating means and standard deviations (M ± SD) of memory test results in the experimental and the control
group. Signi? cant differences are indicated in italics (p < 0.05).
EXPLICIT MEMORY (VERBAL)
3.1 ± 1.7
3.0 ± 2.0
1.5 ± 0.9
8.7 ± 2.0
EXPLICIT MEMORY (SPATIAL)
20.7 ± 4.7
17.5 ± 4.5
2.5 ± 0.7
3.0 ± 0.4
31.9 ± 11.8
42.1 ± 12.4
Perceptual priming1 0.48
0.43 ± 0.19
Contextual priming2 158
178 ± 124
Rating difference score
1.15 ± 1.9
?0.75 ± 2.0
Rating score positive character
?0.08 ± 1.5
?0.50 ± 1.3
Rating score negative character
?1.23 ± 1.9
0.25 ± 1.5
1Difference in fragmentation level between old and new items.
2RT difference between new and old displays in the second half of the experiment.
3One-sample test, test value = 0.
346 and consequently, better object recognition. A paired Student contextual cueing was indistinguishable between the aware and the 377
347 t-test revealed a signi? cant difference in mean fragmentation unaware group. Thus, subjects who reported being aware of display 378
348 levels between previously seen objects (i.e., old) and new objects repetitions were not excluded from the analysis. The results indicate 379
349 [t(34) = 18.0, p < 0.001], with signi? cant facilitation for old items. that memory for context was implicit, but nevertheless facilitated 380
350 Priming scores were calculated by subtracting the level of object search performance. The magnitude of this effect did not differ 381
351 fragmentation of old and new items. The amount of priming did between groups of stressed and unstressed subjects, implying a 382
352 not differ between stressed and unstressed subjects.
lack of stress effects on implicit contextual learning.
353 Contextual priming
354 To measure learning effects, reaction times of correct responses were 25 subjects reported that they were not aware of anything unusual 385
355 analysed (mean response accuracy was 98%). A repeated measures during the presentation of the two CS Pokemon characters, even 386
356 ANOVA revealed a signi? cant interaction between “Display Type” when presented with the names of these characters. The remaining 387
357 (old vs. new displays) and “Epoch” (epoch 1–4) (F[3, 102] = 6.6, 10 subjects (6 stressed, 4 controls) were excluded from data analysis 388
358 p < 0.001), indicating context-dependent learning. Following the due to CS-US covariation awareness of at least one of the two types 389
359 convention by Chun and Jiang (1998), the magnitude of contextual of critical pairings. Difference scores were calculated between CS 390
360 learning was de? ned as the difference in performance between old pos and CS neg ratings. These scores differed signi? cantly between 391
361 and new display conditions over the latter half of the experimental the TSST and the control group [t(23) = 2.4, p = 0.023]. According 392
362 sessions (Epochs 3 and 4). Repeated measures ANOVAs showed a to Student t-tests, difference scores were marginally different from 393
363 main effect of “Display Type” (F[1, 33] = 78.5, p < 0.001), indicat-
zero in the group of subjects exposed to the TSST [t(12) = 2.2, 394
364 ing a signi? cant priming effect but no main effect of stress and no p = 0.051], but not in the control group. A further analysis revealed 395
365 interaction between “Display Type” and “Group” (stress vs. control that conditioning effects in stressed subjects were due to the nega- 396
366 group), suggesting no effect of stress on contextual priming.
tive ratings of the negative Pokemon character (CS neg). The rat- 397
In the post-experimental questionnaire, 15 out of the 35 subjects
ings for this character differed signi? cantly from zero in subjects 398
368 reported that they thought that display repetitions had occurred. exposed to the TSST [t(12) = ?2.3, p = 0.041], but not in the con- 399
369 However, subjects performed at chance in discriminating old dis-
trol subjects (see Figure 1). Also, CS neg ratings differed between 400
370 plays from new displays and those never shown in a recognition stressed and control subjects [t(23) = ?2.1, p = 0.047]. In contrast, 401
371 test: Hit rates were indistinguishable from false positive rates in ratings of the positive Pokemon character (CS pos) did not differ 402
372 the total sample and in a subsample of subjects who reported that from zero in either condition, nor between the two experimental 403
373 they had noticed the repetitions. Subjects who reported being aware groups (see Figure 1). Hence, the conditioning effects observed 404
374 of repetitions did not differ from the remaining subjects in a dis-
in stressed subjects were due to valence speci? c stimulus process- 405
375 play recognition test: No between group differences were found in ing, with a bias towards negative stimuli. The speci? c Pokemon 406
376 hit rates, nor in false positive rates. In addition, the magnitude of character that was paired with the positive US (i.e., the CS pos) 407
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consolidation might have balanced out potentially impairing effects 444
Pokemon Rating Scores
on retrieval. It could be speculated that a stress-induced enhance- 445
ment of consolidation processes during the retention interval may 446
account for the performance increase in the stress group for the 447
spatial explicit memory test. However, consolidation mechanisms 448
are believed to occur over hours (Morris, 2006), even days, and 449
therefore the short delay taking place in our study for the different 450
tasks between training and testing might have not be suf? cient for 451
potential stress effects on consolidation to take place. Alternatively, 452
the stress and cortisol levels induced in our study may have not 453
been strong enough to disrupt memory retrieval.
Our data support previous evidence indicating a clear impair- 455
ment of verbal working memory after stress (Lupien et al., 1999; Oei 456
et al., 2006; Robinson et al., 2008; Schoofs et al., 2008). We found 457
that exposure to a social stressor impaired working memory per- 458
formance. This is in line with the notion that stress affects abilities 459
that require conscious, effortful information processing and there- 460
FIGURE 1 | Pokemon rating scores for CS pos and CS neg in stressed and
fore reduces cognitive ef? ciency. However, within the framework of 461
a general adaptation to stress, it might be indeed an adaptive proc- 462
ess compensated for by increased automatic processing ef? ciency 463
408 or negative US (i.e., the CS neg) had no effect. Neither the rating in the case of important stimuli, such as potentially negative and 464
409 difference score, nor the ratings for the CS pos or the CS neg were threatening events (de Kloet et al., 1999). These processes might 465
410 different for the two Pokemon characters.
be mediated by the release of stress hormones such as cortisol. 466
However, such a mechanism could be potentially maladaptive in 467
conditions of chronic stress and could, therefore, be involved in 468
412 The goal of this study was to investigate the effects of stress and cor-
the development and maintenance of psychiatric conditions such 469
413 tisol on a comprehensive variety of memory tasks, including tests as depression, post traumatic stress disorder (PTSD) and phobias 470
414 for explicit memory, working memory, and implicit memory, and (Elzinga and Bremner, 2002; Wolf, 2008).
415 with special emphasis on these latter ones. One advantage of our
The main ? nding of this paper concerns the differential stress 472
416 experiment was that all these different memory tasks were assessed effects observed for different implicit memory tests. Perceptual 473
417 in the same experimental procedure, which allowed us to compare priming and contextual priming both involving neutral stimuli 474
418 the impact of stress on different domains of memory. Our results were not affected by stress. These ? ndings are in agreement with 475
419 support the view that working memory is sensitive to disruption previous work reporting an absence of stress effects in implicit 476
420 under our experimental conditions (note that both learning and memory (Kirschbaum et al., 1996; Lupien et al., 1997). However, 477
421 recall of explicit learning took place within the hour following the contextual cueing task which is thought to be dependent upon 478
422 stress application). In contrast verbal episodic memory was not hippocampal functioning (Chun and Phelps, 1999; Greene et al., 479
423 affected by stress, while spatial episodic memory was enhanced. We 2007) was also unaffected by the stress manipulation. As in the case 480
424 found no effect of stress on implicit learning for neutral stimuli. of explicit verbal memory, an explanation may be that both study 481
425 However, our results showed an enhancement of implicit memory and test phase were administered under stressful conditions and that 482
426 for negative, but not positive, emotional stimuli. This latter result any facilitating effect of stress at encoding may have been levelled 483
427 is particularly relevant since it suggests a mood congruency effect out by interfering effects at retrieval. Typically, stress effects are most 484
428 of stress in conditioning.
pronounced when retrieval in a stress situation is required for infor- 485
Explicit verbal memory was previously documented to be nega-
mation that has been acquired under non-stressful conditions (de 486
430 tively affected by stress and high cortisol levels (Lupien et al., 2005; Quervain et al., 2000, 2003; Het et al., 2005; Roozendaal, 2002).
431 Sauro et al., 2003; Wolf, 2006), with strong evidence indicating that
For the conditioning task, we expected a stress induced modula- 488
432 retrieval processes are particularly vulnerable (de Quervain et al., tion of performance in line with the mood congruency hypothesis 489
433 2000, 2003; Het et al., 2005; Roozendaal, 2002). Stress and glucocor-
(Colombel, 2007). It was reasoned that due to the aversive charac- 490
434 ticoids may have opposing effects on explicit memory consolidation teristics of stress, this effect might be valence-speci? c, with a bias 491
435 and retrieval, with enhancing effects on consolidation and impair-
towards negative stimuli (Bishop, 2007; Wolf, 2008). Conditioning 492
436 ing effects on retrieval (e.g. Beckner et al., 2006; Roozendaal, 2002; effects were observed in stressed but not control subjects. This ? nd- 493
437 Sandi and Pinelo-Nava, 2007; Smeets et al., 2008). In this context, a ing is consistent with studies in animals reporting enhanced con- 494
438 potential role of reconsolidation on the facilitating effects of stress ditioning after stress when using aversive paradigms, such as fear 495
439 on consolidation has been discussed (Lupien and Schramek, 2006). conditioning (Conrad et al., 1999; Cordero et al., 2003a,b; Sandi 496
440 Under our experimental conditions, verbal explicit memory for et al., 2001; Shors, 2001, 2006), as well as fear conditioning in healthy 497
441 emotionally neutral materials was not affected by stress. This could men (Jackson et al., 2006; Zorawski et al., 2006). In our study, con- 498
442 be related to the fact that learning and retrieval occurred under the ditioning effects in stressed subjects were due to the negative rating 499
443 same stressful conditions: Potentially enhancing effects of stress on of the CS neg. In contrast, the rating for the CS pos did not differ 500
Frontiers in Behavioral Neuroscience
January 2009 | Volume 2 | Article 5 | 6
Luethi et al.
Stress effects on memory
501 from zero in stressed subjects. This suggests that stress can enhance cortisol acutely administered to patients undergoing cardiac surgery 558
502 implicit memory for emotional stimuli in a valence-speci? c manner, (Schelling, 2008). On the other hand, prolonged administration of 559
503 with a bias towards negative materials. The processing bias towards stress-equivalent doses of cortisol during intensive care treatment 560
504 negative stimuli might be due to a bias in attention, learning or in was found to reduce the risk for later PTSD (Schelling, 2008). After 561
505 the willingness to report negative attitudes (Bishop, 2007; Rinck and initial consolidation of traumatic experiences (which is likely to be 562
506 Becker, 2005). As in explicit memory, stress or cortisol enhanced enhanced by glucocorticoids), glucocorticoid levels may play a cru- 563
507 implicit memory is likely to be due to enhanced memory consolida-
cial role in controlling the amount of retrieved traumatic memories 564
508 tion (Zorawski et al., 2006). As mentioned above, enhanced auto-
later on. Speci? cally, by the known reducing effects of glucocorti- 565
509 matic cognitive processing during stress could be thought of as both coids on memory retrieval, these hormones may partly interrupt 566
510 an adaptive process and a potentially maladaptive mechanism. The the vicious cycle of retrieving, re-experiencing and reconsolidating 567
511 former holds true from a cognitive resources viewpoint, that is, aversive memories, thereby preventing a further cementation of 568
512 when conscious and effortful processing of information is decreased, the aversive memory trace (de Quervain, 2008). Studies showing 569
513 and more automatic information processing is increased. However, that the preventive effects of glucocorticoid administration are also 570
514 from a clinical viewpoint, the same mechanism could be potentially observed when the treatment starts at the time of the traumatic 571
515 maladaptive, with negative stimuli appearing to be the ones that are event (Schelling et al., 2004; Weis et al., 2006) indicate that such an 572
516 processed more ef? ciently during times of stress. In line with Jackson inhibitory effect of glucocorticoids on memory retrieval may prevail 573
517 et al. (2006) who found similar conditioning effects, we suggest that over their potentially enhancing effect on initial consolidation.
518 the enhancing effects of stress on the formation of implicit negative
In summary, the degree of stress and the enhanced cortisol 575
519 attitudes provide a model of pathological emotional reactions, such levels induced by our experimental conditions were suf? cient to 576
520 as those found in PTSD.
impair working memory, enhance spatial episodic memory, and 577
Interestingly, elevated levels of glucocorticoids have also been to facilitate classical conditioning for aversive stimuli. In contrast, 578
522 discussed as protective agents with regard to the development and they did not affect performance in verbal explicit memory tasks, or 579
523 symptomatology of anxiety disorders, such as PTSD and phobias in implicit learning tasks that involved neutral or positive stimuli. 580
524 (Aerni et al., 2004; de Quervain, 2006, 2008; Soravia et al., 2006). Given the different brain regions which are hypothesized to play a 581
525 However, these studies used explicit, self report measures of anxi-
major role in orchestrating each of these memory tasks, our results 582
526 ety or anxiety related memories. It is possible that glucocorticoids suggest that stress may reduce the ef? ciency of prefrontal cortex 583
527 impair the retrieval of negative or anxiety-related explicit episodic processing (working memory) and yet facilitate the ef? ciency of 584
528 memories, but still enhance implicit learning of negative stimuli, as amygdala processing (aversive conditioning). At the same time, 585
529 suggested by our study and others, who describe enhanced implicit stress did not seem to negatively affect hippocampal processing, as 586
530 memory for trauma-related materials (McNally, 1997). Indeed, required for explicit memory and implicit memory tasks. However, 587
531 memories of PTSD patients are often characterized by vivid, dream-
this is still somewhat speculative as, in the present study, we did 588
532 like ? ashbacks, yet patients ? nd it dif? cult to retrieve speci? c, auto-
not counterbalance the order of the memory tests. Therefore, it 589
533 biographical memories from their past (McNally, 1997).
may be that variations of stress levels across the different memory 590
Hence, stress exposure and glucocorticoids could be thought tests, as well as variations of stress effects across the different proc- 591
535 of as both a protective mechanism as well as a risk factor in the esses involved in each memory test (i.e., encoding, consolidation 592
536 development and maintenance of PTSD. In fact, one could specu-
and retrieval), also contributed to the differential pattern of test 593
537 late that the discrepancy between enhanced implicit and impaired results. Our experiment was designed to test differences between 594
538 explicit processing of anxiety related stimuli might itself be a risk stressed and control subjects and as saliva cortisol levels were still 595
539 factor in PTSD. In accordance with this view, a mnemonic model of signi? cantly enhanced in stressed subjects at the end of the test 596
540 PTSD has been suggested, with a focus on the current memory of procedure, group differences in each task are caused by the stress 597
541 a negative event, as opposed to the event itself (Rubin et al., 2008). manipulation.
542 Psychotherapeutic interventions in PTSD are also in line with such
A limitation of the present study is that only male subjects were 599
543 a discrepancy between implicit and explicit memories in PTSD included since a gender effect has been found in previous studies 600
544 patients, as they often focus on the patient’s memory for the event (e.g., Buchanan and Tranel, 2008; Jackson et al., 2006; Kelly et al., 601
545 and involve re-experiencing the traumatic event (e.g. Ehlers and 2008; Shors et al., 2004; Stark et al., 2006). Future studies including 602
546 Clark, 2008). It is plausible that such interventions reduce discrep-
both men and women will be required to investigate the impact 603
547 ancies between implicit and explicit memories, thereby reducing of sex differences on stress effects on different memory domains 604
548 PTSD symptoms.
(cf., Cahill, 2003; Het et al., 2005).
Another explanation for the protective role of glucocorticoids
Our results support and extend previous ? ndings on the com- 606
550 in PTSD could be that the same type of memory is affected by plexity of effects induced by acute stress. They reinforce the impor- 607
551 glucocorticoids in opposite ways depending on the memory phase tance of delineating the memory type under study when addressing 608
552 exposed. Based on the ? ndings that glucocorticoids enhance mem-
stress and memory interactions (Sandi and Pinelo-Nava, 2007).
553 ory consolidation, it can be assumed that elevated glucocorticoid
554 levels at the time of an aversive experience may contribute to the ACKNOWLEDGEMENT
555 formation (and strength) of traumatic memories. Indeed, a study in The authors would like to thank Clara Rossetti and Coralie 612
556 critically ill patients found that the number of traumatic memories Siegmund for excellent technical assistance. This work was partially 613
557 from the intensive care unit correlated positively with the dose of supported by intramural funding from the EPFL (to C.S.).
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January 2009 | Volume 2 | Article 5 | 7
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